Skip to main content

Advertisement

Log in

Sugarcane Bagasse Hydrothermal Pretreatment Liquors as Suitable Carbon Sources for Hemicellulase Production by Aspergillus niger

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

The aim of this study was to valorize the hemicellulose-rich liquid fraction (liquor) arising from hydrothermal pretreatment of sugarcane bagasse (SCB) through its utilization as an unconventional, soluble carbon source for the production of hemicellulases, namely xylanases and α-L-arabinofuranosidases (ABFases), by Aspergillus niger DCFS11. Through the use of factorial design, pretreatment conditions producing liquors optimized for either early- or late-phase enzyme production were identified. Subsequent deep characterization of liquor components using liquid chromatography and mass spectrometry was performed to identify compounds likely responsible for hemicellulase induction. SCB liquors arising from various pretreatment configurations induced up to 2- and 8.6-fold higher xylanase and ABFase production, respectively, by A. niger DCFS11 than raw SCB substrate owing to the strong inducing potential of arabinosylated xylooligosaccharides and free arabinose solubilized during pretreatment. Notably, unlike the severe pretreatment conditions required for maximum cellulose saccharification and ethanol yields during biomass conversion, low severity and low biomass loading are required if enzyme production from liquor is desired at early-phase growth with no additional detoxification steps. This suggests that for effective application in biorefineries, separate or multi-step processes would be required to optimize both hemicellulase production by A. niger DCFS11 and cellulose digestion. This work demonstrates the potential of hydrothermal pretreatment of lignocellulosic substrates as a tool to increase the production of enzymes by filamentous fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Carvalheiro F, Duarte LC, Gírio FM (2008) Hemicellulose biorefineries: a review on biomass pretreatments. J Sci Ind Res 67:849–864

    CAS  Google Scholar 

  2. Hu F, Ragauskas A (2012) Pretreatment and lignocellulosic chemistry. Bioenerg Res 5:1043–1066

    Article  CAS  Google Scholar 

  3. Michelin M, Polizeli ML, Ruzene DS, Silva DP, Ruiz HA, Vicente AA, Jorge JA, Terenzi HF, Teixeira JA (2012a) Production of xylanase and β-xylosidase from autohydrolysis liquor of corncob using two fungal strains. Bioprocess Biosyst Eng 35:1185–1192

    Article  CAS  PubMed  Google Scholar 

  4. Michelin M, Polizeli ML, Ruzene DS, Silva DP, Vicente AA, Jorge JA, Terenzi HF, Teixeira JA (2012b) Xylanase and β-xylosidase production by Aspergillus ochraceus: new perspectives for the application of wheat straw autohydrolysis liquor. Appl Biochem Biotechnol 166:336–347

    Article  CAS  PubMed  Google Scholar 

  5. Ottenheim C, Verdejo C, Zimmermann W, Chuan J (2014) Hemicellulase production by Aspergillus niger DSM 26641 in hydrothermal palm oil empty fruit bunch hydrolysate and transcriptome analysis. J Biosci Bioeng 118:696–701

    Article  CAS  PubMed  Google Scholar 

  6. Paredes RS, de Barros RR, Inoue H, Yano S, Bon EP (2015) Production of xylanase, α-L-arabinofuranosidase, β-xylosidase, and β-glucosidase by Aspergillus awamori using the liquid stream from hot-compressed water treatment of sugarcane bagasse. Biomass Convers Biorefin 5:299–307

    Article  Google Scholar 

  7. Robl D, Delabona PS, Costa PS, Lima DJ, Rabelo SC, Pimentel IC, Büchli F, Squina FM, Padilla G, Pradella JG (2015) Xylanase production by endophytic Aspergillus niger using pentose-rich hydrothermal liquor from sugarcane bagasse. Biocatal Biotransform 33:175–187

    Article  CAS  Google Scholar 

  8. Johnson E (2016) Integrated enzyme production lowers the cost of cellulosic ethanol. Biofuels Bioprod Biorefin 10:164–174

    Article  CAS  Google Scholar 

  9. Jönsson LJ, Martin C (2016) Pretreatment of lignocellulose: formation of inhibitory by-products and strategies for minimizing their effects. Bioresour Technol 199:103–112

    Article  PubMed  Google Scholar 

  10. Mammam AS, Lee JM, Kim YC, Hwang IT, Park NK, Hwang YK, Chang JS, Hwang JS (2008) Furfural: hemicellulose/xylose derived biochemical. Biofuels Bioprod Biorefin 2:438–454

    Article  Google Scholar 

  11. Zhang X, Hewetson BB, Mosier NS (2015) Kinetics of maleic acid and aluminum chloride catalyzed dehydration and degradation of glucose. Energy Fuel 29:2387–2393

    Article  CAS  Google Scholar 

  12. CONAB (Companhia Nacional de Abastecimento – National Supply Company) (2017) Acompanhamento da safra brasileira de cana-de-açúcar. Segundo levantamento da safra 2017/2018. http://www.conab.gov.br/OlalaCMS/uploads/arquivos/17_08_24_08_59_54_boletim_cana_portugues_-_2o_lev_-_17-18.pdf [October 31, 2017]

  13. Canilha L, Kumar Chandel A, dos Santos Milessi TS, Fernandes Antunes FA, da Costa Freitas WL, das Graças Almeida Felipe M, da Silva SS (2012) Bioconversion of sugarcane biomass into ethanol: an overview about composition, pretreatment methods, detoxification of hydrolysates, enzimatic saccharification and ethanol fermentation. J Biomed Biotechnol 2012:989572

    Article  PubMed  PubMed Central  Google Scholar 

  14. Costa TH, Vega Sanchez ME, Milagres AM, Scheller HV, Ferraz A (2016) Tissue-specific distribution of hemicelluloses in six different sugarcane hybrids as related to cell wall recalcitrance. Biotechnol Biofuels 9:99

    Article  PubMed  PubMed Central  Google Scholar 

  15. de Souza AP, Leite DC, Pattathil A, Hahn M, Buckeridge MS (2013a) Composition and structure of sugarcane cell wall polysaccharides: implications for second-generation bioethanol production. Bioenerg Res 6:564–579

    Article  CAS  Google Scholar 

  16. Morais de Carvalho D, Martinez-Abad A, Evtuguin DV, Colodette JL, Lindström ME, Vilaplana F, Sevastyanova O (2017) Isolation and characterization of acetylated glucuronoarabinoxylan from sugarcane bagasse and straw. Carbohydr Polym 156:223–234

    Article  CAS  PubMed  Google Scholar 

  17. Overend RP, Chornet E (1987) Fractionation of lignocellulosics by steam-aqueous pretreatments. Philos Trans R Soc Lond A 321:523–536

    Article  CAS  Google Scholar 

  18. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2008) Determination of structual carbohydrates and lignin in biomass. NREL Laboratory Analytical Procedures, Golden

  19. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D (2006) Determination of sugars, byproducts, and degradation products in liquid fraction process samples. NREL Laboratory Analytical Procedures, Golden

  20. Council of Europe (2005) Determination of tannins in herbal drugs In: European directorate for the quality of medicines (ed) European Pharmacopoeia 5.0. Strasbourg, France, p 221

  21. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Degtyarenko K, de Matos P, Ennis M, Hastings J, Zbinden M, McNaught A, Alcántara R, Darsow M, Guedj M, Ashburner M (2008) ChEBI: a database and ontology for chemical entities of biological interest. Nucleic Acids Res 36:D344–D350

    Article  CAS  PubMed  Google Scholar 

  23. Klich MA (2002) Identification of common Aspergillus species. Centraalbureau voor Schimmelautures, Utrecht

    Google Scholar 

  24. Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsubé S, Szigeti G, Yaguchi T, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  26. Rosgaard L, Pedersen S, Meyer AS (2007) Comparison of different pretreatment strategies for enzymatic hydrolysis of wheat and barley straw. Appl Biochem Biotechnol 143:284–296

    Article  CAS  PubMed  Google Scholar 

  27. Vegas R, Kabel M, Schols HA, Alonso JL, Parajó JC (2008) Hydrothermal processing of rice husks: effects of severity on product distribution. J Chem Technol Biotechnol 83:965–972

    Article  CAS  Google Scholar 

  28. Ishii T (1997) Structure and functions of feruloylated polysaccharides. Plant Sci 127:111–127

    Article  CAS  Google Scholar 

  29. Williamson G, Kroon PA, Faulds CB (1998) Hairy plant polysaccharides: a close shave with microbial esterases. Microbiology 144:2011–2023

    Article  CAS  PubMed  Google Scholar 

  30. Kabel MA, Bos G, Zeevalking J, Voragen AG, Schols KA (2007) Effect of pretreatment severity on xylan solubility and enzymatic breakdown of the remaining cellulose from wheat straw. Bioresour Technol 98:2034–2042

    Article  CAS  PubMed  Google Scholar 

  31. Chen X, Lawoko M, Heiningen AV (2010) Kinetics and mechanism of autohydrolysis of hardwoods. Bioresour Technol 101:7812–7819

    Article  CAS  PubMed  Google Scholar 

  32. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    Article  CAS  PubMed  Google Scholar 

  33. Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Adv Appl Microbiol 86:199–249

    Article  PubMed  Google Scholar 

  34. Varga J, Frisvad JC, Kocsubé S, Brankovics B, Tóth B, Sziget G, Samson RA (2011) New and revisited species in Aspergillus section Nigri. Stud Mycol 69:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205–226

    Article  CAS  PubMed  Google Scholar 

  36. Milagres AM, Prade RA (1994) Production of xylanases from Penicillium janthinellum and its use in the recovery of cellulosic textile fibers. Enzym Microb Technol 16:627–632

    Article  CAS  Google Scholar 

  37. Flipphi MJ, Visser J, van der Veen P, de Graaff LH (1994) Arabinase gene expression in Aspergillus niger: indications for coordinated regulation. Microbiology 140:2673–2682

    Article  CAS  PubMed  Google Scholar 

  38. Brown NA, Ries LNA, Goldman GH (2014) How nutritional status signalling coordinates metabolism and lignocellulolytic enzyme secretion. Fungal Genet Biol 72:48–63

    Article  CAS  PubMed  Google Scholar 

  39. de Souza WR, Maintan-Alfenas GP, de Gouvêa PF, Brown NA, Savoldi M, Battaglia E, Goldman MH, de Vries RP, Goldman GH (2013b) The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in D-xylose, L-arabinose and steam-exploded sugarcane bagasse. Fungal Genet Biol 60:29–45

    Article  PubMed  Google Scholar 

  40. Kont R, Kurašin M, Teugjas H, Väljamäe P (2013) Strong cellulase inhibitors from the hydrothermal pretreatment of wheat straw. Biotechnol Biofuels 6:135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cao G, Ximenes E, Nichols NN, Frazer SE, Kim D, Cotta MA, Ladisch MR (2015) Bioabatement with hemicellulase supplementation to reduce enzymatic hydrolysis inhibitors. Bioresour Technol 190:412–415

    Article  CAS  PubMed  Google Scholar 

  42. Palmqvist E, Hahn-Hägerdal B, Szengyel Z, Zacchi G, Rèczey K (1997) Simultaneous detoxification and enzyme production of hemicellulose hydrolysates obtained after steam pretreatment. Enzym Microb Technol 20:286–293

    Article  CAS  Google Scholar 

  43. Yu Y, Feng Y, Xu C, Liu J, Li D (2011) Onsite bio-detoxification of steam-exploded corn stover for cellulosic ethanol production. Bioresour Technol 102:5123–5128

    Article  CAS  PubMed  Google Scholar 

  44. Hseu RS, Huang YH (2007) Recombinant xylanases derived from anaerobic fungi, and the relevant sequences, expression vectors and hosts. US Patent 7226772

Download references

Funding

This work was supported by the Brazilian National Council for Scientific and Technological Development (CNPq), the Coordination for the Improvement of Higher Education Personnel (CAPES), the Foundation for Research Support of the Federal District (FAPDF), and the National Center for Agroenergy Research – Brazilian Enterprise for Agricultural Research (EMBRAPA).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caio de Oliveira Gorgulho Silva.

Electronic Supplementary Materials

ESM 1

(PDF 126 kb)

ESM 2

(XLSX 27 kb)

ESM 3

(XLSX 38 kb)

ESM 4

(PDF 910 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Oliveira Gorgulho Silva, C., de Aquino Ribeiro, J.A., Souto, A.L. et al. Sugarcane Bagasse Hydrothermal Pretreatment Liquors as Suitable Carbon Sources for Hemicellulase Production by Aspergillus niger. Bioenerg. Res. 11, 316–329 (2018). https://doi.org/10.1007/s12155-018-9898-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-018-9898-z

Keywords

Navigation